Ellagic acid exerts protective effect in intrastriatal 6-hydroxydopamine rat model of Parkinson's disease: Possible involvement of ERβ/Nrf2/HO-1 signaling

Brain Research

Volumn 1662, Issue , 2017, Pages 23-30

  Baluchnejadmojarad, Tourandokht ^a   Rabiee, Nafiseh ^a   Zabihnejad, Sedigheh ^a   Roghani, Mehrdad ^b  

^a IRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b SHAHED UNIVERSITY   (Iran)

Author keywords

6 Hydroxydopamine; Apoptosis; Ellagic acid; Oxidative stress; Parkinson's disease

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME B; ELLAGIC ACID; ESTROGEN RECEPTOR BETA; HEME OXYGENASE 1; MALONALDEHYDE; OXIDOPAMINE; PROTEIN S100B; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2; AMINE OXIDASE (FLAVIN CONTAINING); ANTIOXIDANT; HEME OXYGENASE; HMOX1 PROTEIN, RAT; NEUROPROTECTIVE AGENT; NFE2L2 PROTEIN, RAT;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; MALE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAT; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA PARS COMPACTA; TREATMENT DURATION; ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; DRUG EFFECTS; METABOLISM; NEOSTRIATUM; SUBSTANTIA NIGRA;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; CORPUS STRIATUM; DOPAMINERGIC NEURONS; ELLAGIC ACID; ESTROGEN RECEPTOR BETA; HEME OXYGENASE (DECYCLIZING); MALONDIALDEHYDE; MODELS, ANIMAL; MONOAMINE OXIDASE; NEOSTRIATUM; NEUROPROTECTIVE AGENTS; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; OXIDOPAMINE; PARKINSON DISEASE; PARS COMPACTA; RATS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA;

EID: 85014371424     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2017.02.021     Document Type: Article

References (67)

1. Afshin-Majd, S., Khalili, M., Roghani, M., Mehranmehr, N., Baluchnejadmojarad, T., Carnosine exerts neuroprotective effect against 6-hydroxydopamine toxicity in hemiparkinsonian rat. Mol. Neurobiol. 51 (2015), 1064–1070.
2. Ahmad, M., Saleem, S., Ahmad, A.S., Yousuf, S., Ansari, M.A., Khan, M.B., Ishrat, T., Chaturvedi, R.K., Agrawal, A.K., Islam, F., Ginkgo biloba affords dose-dependent protection against 6-hydroxydopamine-induced parkinsonism in rats: neurobehavioural, neurochemical and immunohistochemical evidences. J. Neurochem. 93 (2005), 94–104.
3. Akkoyun, H.T., Karadeniz, A., Investigation of the protective effect of ellagic acid for preventing kidney injury in rats exposed to nicotine during the fetal period. Biotech. Histochem. 91 (2016), 108–115.
4. Allbutt, H.N., Henderson, J.M., Use of the narrow beam test in the rat, 6-hydroxydopamine model of Parkinson's disease. J. Neurosci. Methods 159 (2007), 195–202.
5. Arya, A., Sethy, N.K., Singh, S.K., Das, M., Bhargava, K., Cerium oxide nanoparticles protect rodent lungs from hypobaric hypoxia-induced oxidative stress and inflammation. Int. J. Nanomed. 8 (2013), 4507–4520.
6. Baluchnejadmojarad, T., Roghani, M., Evaluation of functional asymmetry in rats with dose-dependent lesions of dopaminergic nigrostriatal system using elevated body swing test. Physiol. Behav. 82 (2004), 369–373.
7. Baluchnejadmojarad, T., Roghani, M., Mafakheri, M., Neuroprotective effect of silymarin in 6-hydroxydopamine hemi-parkinsonian rat: involvement of estrogen receptors and oxidative stress. Neurosci. Lett. 480 (2010), 206–210.
8. Batassini, C., Broetto, N., Tortorelli, L.S., Borsoi, M., Zanotto, C., Galland, F., Souza, T.M., Leite, M.C., Goncalves, C.A., Striatal Injury with 6-OHDA Transiently Increases Cerebrospinal GFAP and S100B. Neural Plast., 2015, 2015, 387028.
9. Beitz, J.M., Parkinson's disease: a review. Front. Biosci. (Schol Ed) 6 (2014), 65–74.
10. Blum, D., Torch, S., Lambeng, N., Nissou, M., Benabid, A.L., Sadoul, R., Verna, J.M., Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: contribution to the apoptotic theory in Parkinson's disease. Prog. Neurobiol. 65 (2001), 135–172.
11. Borah, A., Paul, R., Choudhury, S., Choudhury, A., Bhuyan, B., Das Talukdar, A., Dutta Choudhury, M., Mohanakumar, K.P., Neuroprotective potential of silymarin against CNS disorders: insight into the pathways and molecular mechanisms of action. CNS Neurosci. Ther. 19 (2013), 847–853.
12. Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976), 248–254.
13. Chattopadhyaya, I., Gupta, S., Mohammed, A., Mushtaq, N., Chauhan, S., Ghosh, S., Neuroprotective effect of Spirulina fusiform and amantadine in the 6-OHDA induced Parkinsonism in rats. BMC Complement. Altern. Med., 15, 2015, 296.
14. Chen, S., Le, W., Neuroprotective therapy in Parkinson disease. Am. J.Ther. 13 (2006), 445–457.
15. Ding, Y., Zhang, B., Zhou, K., Chen, M., Wang, M., Jia, Y., Song, Y., Li, Y., Wen, A., Dietary ellagic acid improves oxidant-induced endothelial dysfunction and atherosclerosis: role of Nrf2 activation. Int. J. Cardiol. 175 (2014), 508–514.
16. Dolatshahi, M., Farbood, Y., Sarkaki, A., Mansouri, S.M., Khodadadi, A., Ellagic acid improves hyperalgesia and cognitive deficiency in 6-hydroxidopamine induced rat model of Parkinson's disease. Iran. J. Basic Med. Sci. 18 (2015), 38–46.
17. El-Garhy, A.M., Abd El-Raouf, O.M., El-Sayeh, B.M., Fawzy, H.M., Abdallah, D.M., Ellagic acid antiinflammatory and antiapoptotic potential mediate renoprotection in cisplatin nephrotoxic rats. J. Biochem. Mol. Toxicol. 28 (2014), 472–479.
18. Farbood, Y., Sarkaki, A., Dolatshahi, M., Taqhi Mansouri, S.M., Khodadadi, A., Ellagic acid protects the brain against 6-hydroxydopamine induced neuroinflammation in a rat model of Parkinson's disease. Basic Clin. Neurosci. 6 (2015), 83–89.
19. Farbood, Y., Sarkaki, A., Dianat, M., Khodadadi, A., Haddad, M.K., Mashhadizadeh, S., Ellagic acid prevents cognitive and hippocampal long-term potentiation deficits and brain inflammation in rat with traumatic brain injury. Life Sci. 124 (2015), 120–127.
20. Finberg, J.P., Pharmacology of Rasagiline, a New MAO-B inhibitor drug for the treatment of Parkinson's disease with neuroprotective potential. Rambam Maimonides Med. J., 1, 2010, e0003.
21. Garcia-Nino, W.R., Zazueta, C., Ellagic acid: pharmacological activities and molecular mechanisms involved in liver protection. Pharmacol. Res. 97 (2015), 84–103.
22. Giacoppo, S., Galuppo, M., Montaut, S., Iori, R., Rollin, P., Bramanti, P., Mazzon, E., An overview on neuroprotective effects of isothiocyanates for the treatment of neurodegenerative diseases. Fitoterapia 106 (2015), 12–21.
23. Gu, L., Deng, W.S., Liu, Y., Jiang, C.H., Sun, L.C., Sun, X.F., Xu, Q., Zhou, H., Ellagic acid protects Lipopolysaccharide/D-galactosamine-induced acute hepatic injury in mice. Int. Immunopharmacol. 22 (2014), 341–345.
24. Gustot, A., Gallea, J.I., Sarroukh, R., Celej, M.S., Ruysschaert, J.M., Raussens, V., Amyloid fibrils are the molecular trigger of inflammation in Parkinson's disease. Biochem. J. 471 (2015), 323–333.
25. Hamad, A.-W.R., Al-Momani, W.M., Janakat, S., Oran, S.A., Bioavailability of ellagic acid after single dose administration using HPLC. Pak. J. Nutr. 8 (2009), 1661–1664.
26. Hassoun, E.A., Vodhanel, J., Abushaban, A., The modulatory effects of ellagic acid and vitamin E succinate on TCDD-induced oxidative stress in different brain regions of rats after subchronic exposure. J. Biochem. Mol. Toxicol. 18 (2004), 196–203.
27. Healy-Stoffel, M., Omar Ahmad, S., Stanford, J.A., Levant, B., Differential effects of intrastriatal 6-hydroxydopamine on cell number and morphology in midbrain dopaminergic subregions of the rat. Brain Res. 1574 (2014), 113–119.
28. Hwang, C.K., Chun, H.S., Isoliquiritigenin isolated from licorice Glycyrrhiza uralensis prevents 6-hydroxydopamine-induced apoptosis in dopaminergic neurons. Biosci. Biotechnol. Biochem. 76 (2012), 536–543.
29. Jalali-Nadoushan, M., Roghani, M., Alpha-lipoic acid protects against 6-hydroxydopamine-induced neurotoxicity in a rat model of hemi-parkinsonism. Brain Res. 1505 (2013), 68–74.
30. Jing, X., Wei, X., Ren, M., Wang, L., Zhang, X., Lou, H., Neuroprotective effects of Tanshinone I against 6-OHDA-induced oxidative stress in cellular and mouse model of Parkinson's disease through upregulating Nrf2. Neurochem. Res. 41 (2016), 779–786.
31. Kabiraj, P., Marin, J.E., Varela-Ramirez, A., Zubia, E., Narayan, M., Ellagic acid mitigates SNO-PDI induced aggregation of Parkinsonian biomarkers. ACS Chem. Neurosci. 5 (2014), 1209–1220.
32. Khatri, D.K., Juvekar, A.R., Kinetics of inhibition of monoamine oxidase using curcumin and ellagic acid. Pharmacogn. Mag. 12 (2016), S116–120.
33. Kiasalari, Z., Baluchnejadmojarad, T., Roghani, M., Hypericum perforatum hydroalcoholic extract mitigates motor dysfunction and is neuroprotective in intrastriatal 6-hydroxydopamine rat model of Parkinson's disease. Cell. Mol. Neurobiol. 36 (2016), 521–530.
34. Kiasalari, Z., Khalili, M., Baluchnejadmojarad, T., Roghani, M., Protective effect of oral hesperetin against unilateral striatal 6-hydroxydopamine damage in the rat. Neurochem. Res. 41 (2016), 1065–1072.
35. Kikuchi, G., Yoshida, T., Noguchi, M., Heme oxygenase and heme degradation. Biochem. Biophys. Res. Commun. 338 (2005), 558–567.
36. Kirik, D., Rosenblad, C., Bjorklund, A., Characterization of behavioral and neurodegenerative changes following partial lesions of the nigrostriatal dopamine system induced by intrastriatal 6-hydroxydopamine in the rat. Exp. Neurol. 152 (1998), 259–277.
37. Koppula, S., Kumar, H., More, S.V., Kim, B.W., Kim, I.S., Choi, D.K., Recent advances on the neuroprotective potential of antioxidants in experimental models of Parkinson's disease. Int. J. Mol. Sci. 13 (2012), 10608–10629.
38. Li, W., Kong, A.N., Molecular mechanisms of Nrf2-mediated antioxidant response. Mol. Carcinog. 48 (2009), 91–104.
39. Macchi, B., Di Paola, R., Marino-Merlo, F., Felice, M.R., Cuzzocrea, S., Mastino, A., Inflammatory and cell death pathways in brain and peripheral blood in Parkinson's disease. CNS Neurol. Disord.: Drug Targets 14 (2015), 313–324.
40. Mansouri, M.T., Farbood, Y., Naghizadeh, B., Shabani, S., Mirshekar, M.A., Sarkaki, A., Beneficial effects of ellagic acid against animal models of scopolamine- and diazepam-induced cognitive impairments. Pharm. Biol. 54 (2016), 1947–1953.
41. Morroni, F., Tarozzi, A., Sita, G., Bolondi, C., Zolezzi Moraga, J.M., Cantelli-Forti, G., Hrelia, P., Neuroprotective effect of sulforaphane in 6-hydroxydopamine-lesioned mouse model of Parkinson's disease. Neurotoxicology 36 (2013), 63–71.
42. Muangpaisan, W., Mathews, A., Hori, H., Seidel, D., A systematic review of the worldwide prevalence and incidence of Parkinson's disease. J. Med. Assoc. Thai. 94 (2011), 749–755.
43. Negahdar, F., Mehdizadeh, M., Joghataei, M.T., Roghani, M., Mehraeen, F., Poorghayoomi, E., Berberine chloride pretreatment exhibits neuroprotective effect against 6-hydroxydopamine-induced neuronal insult in rat. Iran. J. Pharm. Res. 14 (2015), 1145–1152.
44. Nejad, K.H., Dianat, M., Sarkaki, A., Naseri, M.K., Badavi, M., Farbood, Y., Ellagic acid improves electrocardiogram waves and blood pressure against global cerebral ischemia rat experimental models. Electron. Phys. 7 (2015), 1153–1162.
45. Obeso, J.A., Olanow, C.W., Nutt, J.G., Levodopa motor complications in Parkinson's disease. Trends Neurosci. 23 (2000), S2–7.
46. Panahian, N., Yoshiura, M., Maines, M.D., Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J. Neurochem. 72 (1999), 1187–1203.
47. Papoutsi, Z., Kassi, E., Tsiapara, A., Fokialakis, N., Chrousos, G.P., Moutsatsou, P., Evaluation of estrogenic/antiestrogenic activity of ellagic acid via the estrogen receptor subtypes ERalpha and ERbeta. J. Agric. Food Chem. 53 (2005), 7715–7720.
48. Paxinos, G., Watson, C., The Rat Brain in Stereotaxic Coordinates. 2nd ed, 1986, Academic Press, San Diego.
49. Reglodi, D., Renaud, J., Tamas, A., Tizabi, Y., Socias, S.B., Del-Bel, E., Raisman-Vozari, R., Novel tactics for neuroprotection in Parkinson's disease: role of antibiotics, polyphenols and neuropeptides. Prog. Neurobiol. pii, S0301–0082, 2015 00128-8.
50. Ren, W.Q., Tian, Z.M., Yin, F., Sun, J.Z., Zhang, J.N., Extracellular alpha-synuclein–a possible initiator of inflammation in Parkinson's disease. Pharmazie 71 (2016), 51–55.
51. Rodriguez-Oroz, M.C., Jahanshahi, M., Krack, P., Litvan, I., Macias, R., Bezard, E., Obeso, J.A., Initial clinical manifestations of Parkinson's disease: features and pathophysiological mechanisms. Lancet Neurol. 8 (2009), 1128–1139.
52. Rodriguez-Pallares, J., Parga, J.A., Joglar, B., Guerra, M.J., Labandeira-Garcia, J.L., The mitochondrial ATP-sensitive potassium channel blocker 5-hydroxydecanoate inhibits toxicity of 6-hydroxydopamine on dopaminergic neurons. Neurotox. Res. 15 (2009), 82–95.
53. Roghani, M., Behzadi, G., Baluchnejadmojarad, T., Efficacy of elevated body swing test in the early model of Parkinson's disease in rat. Physiol. Behav. 76 (2002), 507–510.
54. Sánchez-González, C., Ciudad, C., Noé, V., Izquierdo-Pulido, M., Health benefits of walnut polyphenols: an exploration beyond their lipid profile. Crit. Rev. Food Sci. Nutr., 29, 2015.
55. Schwarting, R.K., Huston, J.P., Behavioral and neurochemical dynamics of neurotoxic meso-striatal dopamine lesions. Neurotoxicology 18 (1997), 689–708.
56. Sedaghat, R., Roghani, M., Khalili, M., Neuroprotective effect of thymoquinone, the nigella sativa bioactive compound, in 6-hydroxydopamine-induced hemi-parkinsonian rat model. Iran. J. Pharm. Res. 13 (2014), 227–234.
57. Sepand, M.R., Ghahremani, M.H., Razavi-Azarkhiavi, K., Aghsami, M., Rajabi, J., Keshavarz-Bahaghighat, H., Soodi, M., Ellagic acid confers protection against gentamicin-induced oxidative damage, mitochondrial dysfunction and apoptosis-related nephrotoxicity. J. Pharm. Pharmacol. 68 (2016), 1222–1232.
58. Shughrue, P.J., Lane, M.V., Merchenthaler, I., Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J. Comp. Neurol. 388 (1997), 507–525.
59. Spittau, B., Transforming growth factor beta1-mediated anti-inflammation slows progression of midbrain dopaminergic neurodegeneration in Parkinson's disease?. Neural Regen. Res. 10 (2015), 1578–1580.
60. Syapin, P.J., Regulation of haeme oxygenase-1 for treatment of neuroinflammation and brain disorders. Br. J. Pharmacol. 155 (2008), 623–640.
61. Tobon-Velasco, J.C., Vazquez-Victorio, G., Macias-Silva, M., Cuevas, E., Ali, S.F., Maldonado, P.D., Gonzalez-Trujano, M.E., Cuadrado, A., Pedraza-Chaverri, J., Santamaria, A., S-allyl cysteine protects against 6-hydroxydopamine-induced neurotoxicity in the rat striatum: involvement of Nrf2 transcription factor activation and modulation of signaling kinase cascades. Free Radic. Biol. Med. 53 (2012), 1024–1040.
62. Uzar, E., Alp, H., Cevik, M.U., Firat, U., Evliyaoglu, O., Tufek, A., Altun, Y., Ellagic acid attenuates oxidative stress on brain and sciatic nerve and improves histopathology of brain in streptozotocin-induced diabetic rats. Neurol. Sci. 33 (2012), 567–574.
63. Vomhof-Dekrey, E.E., Picklo, M.J. Sr., The Nrf2-antioxidant response element pathway: a target for regulating energy metabolism. J. Nutr. Biochem. 23 (2012), 1201–1206.
64. Wojtunik-Kulesza, K.A., Oniszczuk, A., Oniszczuk, T., Waksmundzka-Hajnos, M., The influence of common free radicals and antioxidants on development of Alzheimer's Disease. Biomed. Pharmacother. 78 (2016), 39–49.
65. Yan, L., Yin, P., Ma, C., Liu, Y., Method development and validation for pharmacokinetic and tissue distributions of ellagic acid using ultrahigh performance liquid chromatography-tandem mass spectrometry (UPLC-MS/MS). Molecules 19 (2014), 18923–18935.
66. Yuan, H., Sarre, S., Ebinger, G., Michotte, Y., Histological, behavioural and neurochemical evaluation of medial forebrain bundle and striatal 6-OHDA lesions as rat models of Parkinson's disease. J. Neurosci. Methods 144 (2005), 35–45.
67. Zare, K., Eidi, A., Roghani, M., Rohani, A.H., The neuroprotective potential of sinapic acid in the 6-hydroxydopamine-induced hemi-parkinsonian rat. Metab. Brain Dis. 30 (2015), 205–213.